Evolutionary analysis identifies a Golgi pathway and correlates lineage-specific factors with endomembrane organelle emergence in apicomplexans

• Published in: Cell reports (Cambridge) 2024-02, Vol.43 (2), p.113740-113740, Article 113740
• Main Authors: Klinger, Christen M., Jimenez-Ruiz, Elena, Mourier, Tobias, Klingl, Andreas, Lemgruber, Leandro, Pain, Arnab, Dacks, Joel B., Meissner, Markus
• Format: Article
• Language: English
• Subjects: Apicomplexa; Arl; CP: Cell biology; evolution; evolutionary cell biology; Golgi; membrane trafficking; molecular evolution; phylogenetic screen; Toxoplasma; Toxoplasma gondii
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2024.113740

The organelle paralogy hypothesis (OPH) aims to explain the evolution of non-endosymbiotically derived organelles. It predicts that lineage-specific pathways or organelles should result when identity-encoding membrane-trafficking components duplicate and co-evolve. Here, we investigate the presence of such lineage-specific membrane-trafficking machinery paralogs in Apicomplexa, a globally important parasitic lineage. We are able to identify 18 paralogs of known membrane-trafficking machinery, in several cases co-incident with the presence of new endomembrane organelles in apicomplexans or their parent lineage, the Alveolata. Moreover, focused analysis of the apicomplexan Arf-like small GTPases (i.e., ArlX3) revealed a specific post-Golgi trafficking pathway. This pathway appears involved in delivery of proteins to micronemes and rhoptries, with knockdown demonstrating reduced invasion capacity. Overall, our data have identified an unforeseen post-Golgi trafficking pathway in apicomplexans and are consistent with the OPH mechanism acting to produce endomembrane pathways or organelles at various evolutionary stages across the alveolate lineage. [Display omitted] •Many lineage-specific membrane-trafficking paralogs exist in the apicomplexans•Myzozoan-specific ArlX3 mediates post-Golgi transport to micronemes and rhoptries•Emergence of paralogs coincides with new organelles or pathways in this lineage Unique membrane-trafficking pathways or organelles are proposed to coincide with the expansion and specialization of trafficking factors. Using the parasite Toxoplasma gondii as a model system, Klinger et al. identified the myzozoan-specific trafficking factor ArlX3 as critical for post-Golgi transport to unique secretory organelles, micronemes, and rhoptries.